Facilitation of Saccadic Eye Movements by Postsaccadic Electrical Stimulation in the Primate Caudate

Overview

Journal J Neurosci

Specialty Neurology

Date 2006 Dec 15

PMID 17167079

Citations 26

Authors

Kae Nakamura

Okihide Hikosaka

Affiliations

Soon will be listed here.

Abstract

Sensorimotor experience followed by positive feedback leads to motor learning. Although the striatum, an input channel of the basal ganglia, has been implicated to play a key role in motor learning, little is known about how reward information modulates the neuronal processes in the striatum that causes behavioral changes. Here, we report that direct manipulation of the neuronal signal in the primate caudate yields behavioral changes comparable with those induced by natural reward. Electrical stimulation in the oculomotor region of the caudate immediately after saccades to a fixed direction led to selective facilitation of saccades in that direction. The facilitation remained even after stimulation was stopped, indicating a plastic change. These effects were observed when stimulation was applied after, not before, saccades. We propose that the caudate plays a causal role in behavioral changes by integrating selective sensorimotor and reward information in a temporally specific manner.

Citing Articles

Reward signals in the motor cortex: from biology to neurotechnology.

Derosiere G, Shokur S, Vassiliadis P Nat Commun. 2025; 16(1):1307.

PMID: 39900901 PMC: 11791067. DOI: 10.1038/s41467-024-55016-0.

Non-invasive stimulation of the human striatum disrupts reinforcement learning of motor skills.

Vassiliadis P, Beanato E, Popa T, Windel F, Morishita T, Neufeld E Nat Hum Behav. 2024; 8(8):1581-1598.

PMID: 38811696 PMC: 11343719. DOI: 10.1038/s41562-024-01901-z.

Implication of regional selectivity of dopamine deficits in impaired suppressing of involuntary movements in Parkinson's disease.

Lee H, Kim H, Hikosaka O Neurosci Biobehav Rev. 2024; 162:105719.

PMID: 38759470 PMC: 11167649. DOI: 10.1016/j.neubiorev.2024.105719.

Organization of reward and movement signals in the basal ganglia and cerebellum.

Larry N, Zur G, Joshua M Nat Commun. 2024; 15(1):2119.

PMID: 38459003 PMC: 10923830. DOI: 10.1038/s41467-024-45921-9.

Neural Representations of Post-Decision Accuracy and Reward Expectation in the Caudate Nucleus and Frontal Eye Field.

Fan Y, Doi T, Gold J, Ding L J Neurosci. 2023; 44(2).

PMID: 37963761 PMC: 10860634. DOI: 10.1523/JNEUROSCI.0902-23.2023.

References

Kawagoe R, Takikawa Y, Hikosaka O . Expectation of reward modulates cognitive signals in the basal ganglia. Nat Neurosci. 1999; 1(5):411-6. DOI: 10.1038/1625. View

Paladini C, Celada P, Tepper J . Striatal, pallidal, and pars reticulata evoked inhibition of nigrostriatal dopaminergic neurons is mediated by GABA(A) receptors in vivo. Neuroscience. 1999; 89(3):799-812. DOI: 10.1016/s0306-4522(98)00355-8. View

Charpier S, Mahon S, Deniau J . In vivo induction of striatal long-term potentiation by low-frequency stimulation of the cerebral cortex. Neuroscience. 1999; 91(4):1209-22. DOI: 10.1016/s0306-4522(98)00719-2. View

Iribe Y, Moore K, Pang K, Tepper J . Subthalamic stimulation-induced synaptic responses in substantia nigra pars compacta dopaminergic neurons in vitro. J Neurophysiol. 1999; 82(2):925-33. DOI: 10.1152/jn.1999.82.2.925. View

Jog M, Kubota Y, Connolly C, Hillegaart V, Graybiel A . Building neural representations of habits. Science. 1999; 286(5445):1745-9. DOI: 10.1126/science.286.5445.1745. View

Phillips A, Mora F, Rolls E . Intracranial self-stimulation in orbitofrontal cortex and caudate nucleus of rhesus monkey: effects of apomorphine, pimozide, and spiroperidol. Psychopharmacology (Berl). 1979; 62(1):79-82. DOI: 10.1007/BF00426039. View

Hikosaka O, Takikawa Y, Kawagoe R . Role of the basal ganglia in the control of purposive saccadic eye movements. Physiol Rev. 2000; 80(3):953-78. DOI: 10.1152/physrev.2000.80.3.953. View

Reynolds J, Wickens J . Substantia nigra dopamine regulates synaptic plasticity and membrane potential fluctuations in the rat neostriatum, in vivo. Neuroscience. 2000; 99(2):199-203. DOI: 10.1016/s0306-4522(00)00273-6. View

Partridge J, Tang K, Lovinger D . Regional and postnatal heterogeneity of activity-dependent long-term changes in synaptic efficacy in the dorsal striatum. J Neurophysiol. 2000; 84(3):1422-9. DOI: 10.1152/jn.2000.84.3.1422. View

10.

Miller E, Cohen J . An integrative theory of prefrontal cortex function. Annu Rev Neurosci. 2001; 24:167-202. DOI: 10.1146/annurev.neuro.24.1.167. View

11.

Hassani O, Cromwell H, Schultz W . Influence of expectation of different rewards on behavior-related neuronal activity in the striatum. J Neurophysiol. 2001; 85(6):2477-89. DOI: 10.1152/jn.2001.85.6.2477. View

12.

Reynolds J, Hyland B, Wickens J . A cellular mechanism of reward-related learning. Nature. 2001; 413(6851):67-70. DOI: 10.1038/35092560. View

13.

Takikawa Y, Kawagoe R, Hikosaka O . Reward-dependent spatial selectivity of anticipatory activity in monkey caudate neurons. J Neurophysiol. 2002; 87(1):508-15. DOI: 10.1152/jn.00288.2001. View

14.

Lauwereyns J, Takikawa Y, Kawagoe R, Kobayashi S, Koizumi M, Coe B . Feature-based anticipation of cues that predict reward in monkey caudate nucleus. Neuron. 2002; 33(3):463-73. DOI: 10.1016/s0896-6273(02)00571-8. View

15.

White N, McDonald R . Multiple parallel memory systems in the brain of the rat. Neurobiol Learn Mem. 2002; 77(2):125-84. DOI: 10.1006/nlme.2001.4008. View

16.

Packard M, Knowlton B . Learning and memory functions of the Basal Ganglia. Annu Rev Neurosci. 2002; 25:563-93. DOI: 10.1146/annurev.neuro.25.112701.142937. View

17.

Lauwereyns J, Watanabe K, Coe B, Hikosaka O . A neural correlate of response bias in monkey caudate nucleus. Nature. 2002; 418(6896):413-7. DOI: 10.1038/nature00892. View

18.

Miyachi S, Hikosaka O, Lu X . Differential activation of monkey striatal neurons in the early and late stages of procedural learning. Exp Brain Res. 2002; 146(1):122-6. DOI: 10.1007/s00221-002-1213-7. View

19.

Canales J, Capper-Loup C, Hu D, Choe E, Upadhyay U, Graybiel A . Shifts in striatal responsivity evoked by chronic stimulation of dopamine and glutamate systems. Brain. 2002; 125(Pt 10):2353-63. DOI: 10.1093/brain/awf239. View

20.

Reynolds J, Wickens J . Dopamine-dependent plasticity of corticostriatal synapses. Neural Netw. 2002; 15(4-6):507-21. DOI: 10.1016/s0893-6080(02)00045-x. View